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Complex Hybridity in Isotoma Petraea V. Allozyme

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Complex Hybridity in Isotoma Petraea V. Allozyme Heredity (1983) 51 (3), 653—663 1983. The Genetical Society of Great Britain COMPLEXHYBRIDITY IN ISOTOMA PETRAEA V. ALLOZYME VARIATION AND THE PURSUIT OF HYBRIDITY S. H. JAMES,* A. P. WYLIE,t M. S. JOHNSON* S. A. CARSTAIRS* AND G. A. SIMPSON* * Department of Botany, University of Western Australia, Nedlands, 6009, Australia; t Department of Botany, University of Otago, Dunedin, New Zealand; Department of Zoology, University of Western Australia, Nedlands, 6009, Australia Received13.vi.83 SUMMARY Isoenzymeanalysis of 12 structurally homozygous and 24 complex hybrid popula- tion samples of Isotoma petraea for ten enzyme systems revealed 9 polymorphic and 4 monomorphic loci. The structurally homozygous populations were rela- tively depauperate in allozyme heterozygotes so that rare alleles occurred more frequently as homozygous rather than heterozygous genotypes. The com- plex hybrid populations exhibited high levels of fixed allozymic hybridity and were 12'S times as heterozygous at these loci as were the structural homozygotes. The distribution of allozymic variability supports the theory that complex hybridity in Isotoma originated on Pigeon Rock and migrated through the Isotoma population system to the south-west. Evidence was also adduced that during the evolution of the larger ringed complex hybrids, allozyme homozygosity sometimes replaced allozyme heterozygosity although the segments which carried these loci remained, indubitably, in fixed heterozygosity. 1. INTRODUCTION Isotomapetraea is a herbaceous perennial and mainly self-pollinating member of the Lobeliaceae endemic to granite outcrops and other rocky areas throughout the Eremaean Province of Australia. The species is of particular interest in that, in the south—western corner of its distributional range, it has evolved complex hybridity (James 1965, 1970). It exists in small isolated populations between which there is little migration. Complex hydridity evidently arose on Pigeon Rock, a large granite outcrop some 145 km north of Southern Cross in Western Australia. The genetic system has spread from that location in a generally south-westerly direction so that the multiple interchange ring, initially 06 at Pigeon Rock, has enlarged through a sequence of intermediate sizes, to 014 in extreme south-westerly popula- tions. The evolution of complex hybridity in Isotoma has been taken to represent a clear demonstration of natural selection acting as a force directing the orthogenetic assembly of increasingly conservative devices in a "pursuit of hybridity" (Darlington 1958), following the adoption of an autogamous breeding mechanism (James 1965, 1970). Levy and Levin (1975) point out that there is "general agreement that complex structural hybridity arose as a mechanism that preserves or accumu- lates genic heterozygosity in unspecific or hybridising populations originally Previous paper in series: Beltran, 1. C. and S. H. James (1974), Complex Hydridity in Isotoma petraea. IV. heterosis in interpopulational hybrids. Aust. J. Bot. 22, 25 1—264. 653 654 S. H. JAMES ET AL. adapted to outbreeding but more recently subject to inbreeding by virtue of self-compatibility or small population size.... Therefore, relative to bivalent forms, structurally heterozygous species ought to be highly heterozygous genetically and, correlatively, should exhibit a large propor- tion of polymorphic loci with a rich array of alleleic variants". Their analysis of allozyme variation in the Oenothera biennis complex, however, showed that "When compared to plant species in general, the permanent transloca- tion heterozygotes. .. aregenically depauperate and display only moderate levels of genic heterozygosity" although individual lineages were able "to maintain genic heterozygosity in spite of enforced self -fertilisation for more than 20 generations" in culture. They conclude that "This ability, rather than extraordinarily high levels of heterozygosity per se, distinguishes the ring-forming oenotheras from typical self-fertilising plants". Levin (1975) suggests that "The advent of electrophoretic techniques has permitted the testing of long-standing hypothesis in Oenothera and it is evident that some foregone conclusions about gene-chromosome relation- ships need to be reconsidered". Levy and Levin (1975) "view the origin of complex structural hybridity in Oenothera as the result of selection for increased fertility in areas of hybridisation between taxa differing by several segmental arrangements. The greatest fertility and thus fitness would accrue to hybrids which had the lowest incidence of duplicate and deficient gametes". They suggest that "The view that complex structural hybridity is a means to escape sterility is consistent with the depauperate gene pools of each species and the Oe. biennis complex as a whole, the high level of genetic identity among taxa, and the large number of homogyzous ring-forming strains". On the other hand, the evolution of complex hybridity in Isotoma petraea has been interpreted, holistically, in terms of a "pursuit of hybridity" (vide supra). Heterozygote advantage would appear to be the only basis upon which natural selection could displace apparently fully fertile structural homozygotes with ring-of-fourteen complex heterozygotes exhibiting 90 per cent sterility (James, 1970). The very high levels of sterility in Isotoma complex hybrids would certainly seem to preclude an "escape from sterility" as a basis for their selective advantage. In this paper, starch gel electrophoretic procedures for 10 enzyme systems in Isotoma are reported. They permit the identification of 13 loci, of which 9 were polymorphic. Two cases of electrophenotypic variation which may be due to post-translational effects are noted. These techniques enabled a useful comparison of the genetic variation in primitive structural homozygote populations with that of their complex hybrid derivatives, and indicate a basis for compromise between the two contending evolutionary hypotheses. 2. MATERIAL AND METHODS A collection of 490 plants from 36 south-western populations of Isotoma petraea was grown from cuttings under ambient glasshouse conditions, but in a few cases, seedling progenies were used in place of field collected cutting material. A single young unopened flower bud (diploid tissue) or the pollen from 3 to 6 freshly opened flowers (haploid tissue) was homogenised in 75 l COMPLEX HYBRIDITY IN ISOTOMA 655 of 10 per cent sucrose containing 05 per cent bromo-phenol blue and a trace of Cleland's reagent (DTT: dithioerythritol) in microtitration wells at about 0—4°C. Homogenates were absorbed into 6 x 4 mm Whatman No. 1 Chromatography paper wicks, blotted on filter paper and inserted into 125percent starch gels (Electrostarch or Connaught) for flat-bed elec- trophoresis. The gels supported an ice tray for additional cooling and were run in a refrigerator at 4°C until the dye front had moved about 8 cm. Two buffer systems were used (a) Lithiumborate: modifiedfrom buffer system 2. Lithium hydroxide, Selander eta!., (1971). Electrode buffer: 0 19 M boric acid, 003 M Lithium hydroxide. Gel buffer: 045 M Tris, 0072 M citric acid. Gel: combine 35 ml of Gel buffer and 15 ml of Electrode buffer with water to 250 ml. 250 V, 80 mA. (GOT, LAP, EST, PGI). (b) Tris citrate:modifiedfrom buffer system 4. Continuous tris citrate, Selander et al., (1971). Electrode buffer: 0223 M Tris, 0086 M citric acid, 0.01 M MgCI2, pH 70. Gel: 1: 85 dilution of electrode buffer. 150 V, 80 mA. (ADH, GDH, IDH, PGM, 6PGD, ShDH). All the enzymes demonstrated in these studies migrate anodally. Specific staining for activity within the gel was obtained using the recipes of Shaw and Prasad (1979) except that 1 per cent agar overlays were used instead of liquid incubations in all assays using tetrazolium salts apart from GDH. Invariably, we used MTT(3-(4,5-dimethylthiazolyl-2)-2,5-diphenyl tetrazolium bromide) as the tetrazolium salt. ShDH was assayed by the method in Linhart et aL, (1981). Following staining, overlain gels were stopped by smearing with 45 per cent acetic acid. Gels were fixed for 30 minutes by immersion in 7 per cent acetic acid, washed in distilled water, impregnated with 5 per cent glycerol for 30 minutes, wrapped in cellophane and dried according to the method of Numachi (1981) as permanent records. 3. RESULTS AND INTERPRETATIONS (I) The enzyme systems used (a) PGI (Phosphoglucoisomerase): This enzyme regularly displayed two zones of activity in diploid tissue and pollen homogenates, corre- sponding to two loci, .PGI-1 and PGI-2. Both loci were monomorphic. (b) ADH (Alcohol dehydrogenase): ADH phenotypes consist of a single band at either of two positions, or two bands, one at each position, in both diploid and haploid materials. The enzyme appears to be more abundant in pollen than in bud homogenates. ADH in isotoma is a monomeric enzyme coded by a single locus at which we have observed two alleles. (c) GOT (Glutamate oxaloacetate transaminase):GOTisoenzymes are coded by 4 loci in this material (fig. 1). GOT-i,thefastest, is 656 S. H. JAMES ET AL. expressed in both diploid tissue and pollen, and is presumably of cytoplasmic occurrence. It is polymorphic, with 3 alleles being recorded, the fastest being GOT-i 1. Heterozygotes produce a blurred zone of activity because of their heteromer products, but those of GOT- 1(1/3) which combine the most widely spaced allo- zymes, exhibit a fairly distinct middle band in diploid zymograms. In pollen zymograms, the middle band is not present due to meiotic segregation
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